Inhibitory Circuits Accounting for Development of Visual Cortical Mappings, Stimulus Preferences, and Psychophysical Performance

Abstract

A developmental rationale is proposed for the circuitry underlying the generation of fine retinotopic mappings, the quantitative range of simple-cell stimulus preferences, and the psychophysical performance of the visual system. It is assumed that the retina consists of a mosaic of partially overlapping elements, or hyperfields, which are laid down in a sunflower-seed pattern. These hyperfields project to a corresponding rectilinear mosaic of hypercolumns in the cortex, according to a pattern of chemoaffinities. Each hyperfield, in turn, consists of a sunflower-seed mosaic of nonoverlapping ganglion-cell receptive-field centres, which project to a matching rectilinear mosaic of minicolumns in the corresponding hypercolumn. Retinotopic order is produced in the hyperfield-hypercolumn mapping by radially symmetric inhibitory links, between cortical cells more than two minicolumns apart, which operate on Hebb-modifiable retinocortical excitatory afferent fibres. Under this mapping, hyperfield radii map onto parallel rows of minicolumns (orientation columns), and concentric semicircles of ganglion-cell receptive fields map onto spatial-frequency columns, crossing orientation columns at right angles. The ‘scatter’ in this mapping is equivalent to one local average receptive-field diameter. Orientation-related stimulus preferences are produced by asymmetrical inhibitory links between cells more than two minicolumns apart, in the same spatial-frequency columns. A third network of inhibitory circuits, with Hebb-modifiable synapses, is assumed to operate between cells in the same or immediately adjacent minicolumns. This network enhances stimulus selectivity and sensitivity in simple and hypercomplex cells, and is responsible for adaptation aftereffects and sensory information storage.